diff --git a/homeassistant/components/intent/__init__.py b/homeassistant/components/intent/__init__.py
index 72853276ab3aa..17ec8602d9834 100644
--- a/homeassistant/components/intent/__init__.py
+++ b/homeassistant/components/intent/__init__.py
@@ -615,7 +615,7 @@ async def post(self, request: web.Request, data: dict[str, Any]) -> web.Response
             intent_result = await intent.async_handle(
                 hass, DOMAIN, intent_name, slots, "", self.context(request)
             )
-        except intent.IntentHandleError as err:
+        except (intent.IntentHandleError, intent.MatchFailedError) as err:
             intent_result = intent.IntentResponse(language=language)
             intent_result.async_set_speech(str(err))
 
diff --git a/tests/components/intent/test_init.py b/tests/components/intent/test_init.py
index 3779930e360a8..1993ebe46e40b 100644
--- a/tests/components/intent/test_init.py
+++ b/tests/components/intent/test_init.py
@@ -73,6 +73,32 @@ async def async_handle(self, intent_obj):
     }
 
 
+async def test_http_handle_intent_match_failure(
+    hass: HomeAssistant, hass_client: ClientSessionGenerator, hass_admin_user: MockUser
+) -> None:
+    """Test handle intent match failure via HTTP API."""
+
+    assert await async_setup_component(hass, "intent", {})
+
+    hass.states.async_set(
+        "cover.garage_door_1", "closed", {ATTR_FRIENDLY_NAME: "Garage Door"}
+    )
+    hass.states.async_set(
+        "cover.garage_door_2", "closed", {ATTR_FRIENDLY_NAME: "Garage Door"}
+    )
+    async_mock_service(hass, "cover", SERVICE_OPEN_COVER)
+
+    client = await hass_client()
+    resp = await client.post(
+        "/api/intent/handle",
+        json={"name": "HassTurnOn", "data": {"name": "Garage Door"}},
+    )
+    assert resp.status == 200
+    data = await resp.json()
+
+    assert "DUPLICATE_NAME" in data["speech"]["plain"]["speech"]
+
+
 async def test_cover_intents_loading(hass: HomeAssistant) -> None:
     """Test Cover Intents Loading."""
     assert await async_setup_component(hass, "intent", {})